Fibrillar collagen: The key to vertebrate evolution? A tale of molecular incest

Boot-Handford, Raymond P.; Tuckwell, Danny S.

doi:10.1002/bies.10230

Cited by 173 publications

(139 citation statements)

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“…5 for exon structures through these domains). These unusual molecular features of the collagen XXVII polypeptide have previously only been found in invertebrate fibrillar collagens (7). However, in type XXVII, these features appear to have evolved within the vertebrate lineage after the type C clade diverged from the type B clade (Fig.…”

Section: Discussionmentioning

confidence: 69%

“…The founder vertebrate fibrillar collagen gene acquired an elongated chain selection sequence (7). Gene/genome duplication events led to the evolution of the founder genes for the type A, B, and C clades.…”

Section: Figmentioning

confidence: 99%

“…This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. the puffer fish (Fugu rubripes) genome as duplicates that are conserved yet, at the same time, slowly diverging in sequence (7). It was while identifying fibrillar collagen genes in the puffer fish genome that we discovered a novel fibrillar collagen gene that was not only duplicated within the fish genome but also highly conserved in man and mouse.…”

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confidence: 92%

“…We have recently described how the members of the two clades of vertebrate fibrillar collagens have apparently arisen early during vertebrate evolution from a single founder gene through the mechanism of "molecular incest" (7). Molecular incest is catalyzed by gene/genome duplications, events that not only characterize but are thought by many to have promoted vertebrate evolution (8).…”

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confidence: 99%

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A Novel and Highly Conserved Collagen (proα1(XXVII)) with a Unique Expression Pattern and Unusual Molecular Characteristics Establishes a New Clade within the Vertebrate Fibrillar Collagen Family

Boot-Handford

Tuckwell

Plumb

et al. 2003

Journal of Biological Chemistry

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The type XXVII collagen gene codes for a novel vertebrate fibrillar collagen that is highly conserved in man, mouse, and fish (Fugu rubripes). The pro␣1(XXVII) chain has a domain structure similar to that of the type B clade chains (␣1(V), ␣3(V), ␣1(XI), and ␣2(XI)). However, compared with other vertebrate fibrillar collagens (types I, II, III, V, and XI), type XXVII collagen has unusual molecular features such as no minor helical domain, a major helical domain that is short and interrupted, and a short chain selection sequence within the NC1 domain. Pro␣1(XXVII) mRNA is 9 kb and expressed by chondrocytes but also by a variety of epithelial cell layers in developing tissues including stomach, lung, gonad, skin, cochlear, and tooth. By Western blotting, type XXVII antisera recognized multiple bands of 240 -110 kDa in tissue extracts and collagenous bands of 150 -140 kDa in the conditioned medium of the differentiating chondrogenic ATDC5 cell line. Phylogenetic analyses revealed that type XXVII, together with the closely related type XXIV collagen gene, form a new, third clade (type C) within the vertebrate fibrillar collagen family. Furthermore, the exon structure of the type XXVII collagen gene is similar to, but distinct from, those of the genes coding for the type A or B clade pro␣ chains.Fibril-forming or fibrillar collagens are one of the most ancient families of extracellular matrix molecules being found throughout the metazoan kingdom from the simplest (porifera (sponges)) to the most complex animals (vertebrates). Fibrillar collagens form major structural elements in extracellular matrices as diverse as the evolutionarily "primitive" mesoglea of cnidarians (1) to the highly specialized connective tissues of vertebrates (e.g. bone, cartilage, skin, and tendon) (2). Molecular features shared by all members of this family include a highly conserved C-terminal noncollagenous (NC1) domain and a long collagenous domain of ϳ1000 amino acid residues.Phylogenetic analyses have revealed that the previously known vertebrate fibrillar collagens fall into two related but distinct groups or clades (3, 4). The type A clade consists of the pro␣1(I), pro␣2(I), pro␣1(II), pro␣1(III), and pro␣2(V), whereas the type B clade contains the remaining chains encoding types V and XI collagens (with the exception of pro␣3(XI), which is derived from the COL2A1 gene). The division of the vertebrate fibrillar collagens into two clades is supported by two further observations. Firstly, the exon structures of the genes are virtually identical within a clade yet distinct between clades (5). Secondly, the members of each clade share homologous Nterminal noncollagenous domains (von Willebrand factor type C domain for type A and TSPN 1 for type B clade members) with the exception of the pro␣2(I) chain, where the N-terminal noncollagenous domain appears to have been deleted (6).We have recently described how the members of the two clades of vertebrate fibrillar collagens have apparently arisen early during vertebrate evolution from a single ...

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Section: Discussionmentioning

confidence: 69%

Section: Figmentioning

confidence: 99%

mentioning

confidence: 92%

mentioning

confidence: 99%

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A Novel and Highly Conserved Collagen (proα1(XXVII)) with a Unique Expression Pattern and Unusual Molecular Characteristics Establishes a New Clade within the Vertebrate Fibrillar Collagen Family

Boot-Handford

Tuckwell

Plumb

et al. 2003

Journal of Biological Chemistry

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“…In vertebrates, a short region of the C-propeptide appears to be involved in chain recognition (3). Recently, Boot-Handford and Tuckwell (4) indicated that most of this recognition sequence is absent in all invertebrate fibrillar chains characterized to date. During the extracellular maturation of procollagen molecules, the propeptides are generally removed by specific proteinases.…”

mentioning

confidence: 99%

Invertebrate Data Predict an Early Emergence of Vertebrate Fibrillar Collagen Clades and an Anti-incest Model

Aouacheria

Cluzel

Lethias

et al. 2004

Journal of Biological Chemistry

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Chem. 278, 31067-31077). In this model, a rare genomic event leads to the formation of the founder vertebrate fibrillar collagen gene prior to the early vertebrate genome duplications and the radiation of the vertebrate fibrillar collagen clades (A, B, and C). Here, we present the modular structure of the fibrillar collagen chains present in different invertebrates from the protostome Anopheles gambiae to the chordate Ciona intestinalis. From their modular structure and the use of a triple helix instead of C-propeptide sequences in phylogenetic analyses, we were able to show that the divergence of A and B clades arose early during evolution because ␣ chains related to these clades are present in protostomes. Moreover, the event leading to the divergence of B and C clades from a founder gene arose before the appearance of vertebrates; altogether these data contradict the Boot-Handford model. Moreover, they indicate that all the key steps required for the formation of fibrils of variable structure and functionality arose step by step during invertebrate evolution.Fibrillar collagens are present from sponges to humans and are the primary component of striated fibrils (1, 2). A fibrillar procollagen molecule is made of three identical or different pro-␣ chains. Each pro-␣ chain contains a central triple helix made of ϳ338 Gly-Xaa-Yaa triplets flanked by non-collagenous telopeptide regions, which in turn are flanked by the N-and C-propeptides. The C-propeptide is known to contain the most conserved regions of the fibrillar ␣ chains. This domain is involved in ␣ chain recognition and in the registration of the major triple helical domain, an important step preceding elongation of the triple helix from the carboxyl to the amino terminus. In vertebrates, a short region of the C-propeptide appears to be involved in chain recognition (3). Recently, Boot-Handford and Tuckwell (4) indicated that most of this recognition sequence is absent in all invertebrate fibrillar chains characterized to date. During the extracellular maturation of procollagen molecules, the propeptides are generally removed by specific proteinases. The resultant collagen molecules participate in fibril formation.In humans, fibrillar collagens are subdivided quantitatively into major (types I-III) and minor (types V/XI) collagens. According to the collagen types incorporated into the fibrils and their ratio, the partial processing of the N-propeptide, and interactions with other extracellular matrix components, the shape and functional properties of the fibrils can vary. The importance of quantitatively minor collagens in the regulation of fibril diameter has been pointed out in several studies (5-7). From the model of Linsenmayer et al. (6), the retention of the type V N-propeptide at the surface of types I/V heterotypic fibrils is one of the key elements regulating the diameter of these fibrils.From phylogenetic studies and the exon/intron organization, it has been shown that vertebrate fibrillar collagens can be divided into two clades (8 -10): the A...

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Collagen fibrillogenesis in tendon development: Current models and regulation of fibril assembly

Banos

Thomas

Kuo

2008

Birth Defects Research Pt C

116

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Tendons are collagen-based fibrous tissues that connect and transmit forces from muscle to bone. These tissues, which are high in collagen type I content, have been studied extensively to understand collagen fibrillogenesis. Although the mechanisms have not been fully elucidated, our understanding has continued to progress. Here, we review two prevailing models of collagen fibrillogenesis and discuss the regulation of the process by candidate cellular and extracellular matrix molecules. Although numerous molecules have been implicated in the regulation of collagen fibrillogenesis, we focus on those that have been suggested to be particularly relevant to collagen type I fibril formation during tendon development, including members of the collagen and small leucine-rich proteoglycan families, as well as other molecules, including scleraxis, cartilage oligomeric matrix protein, and cytoskeletal proteins.

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Fibrillar collagen: The key to vertebrate evolution? A tale of molecular incest

Cited by 173 publications

References 31 publications

A Novel and Highly Conserved Collagen (proα1(XXVII)) with a Unique Expression Pattern and Unusual Molecular Characteristics Establishes a New Clade within the Vertebrate Fibrillar Collagen Family

A Novel and Highly Conserved Collagen (proα1(XXVII)) with a Unique Expression Pattern and Unusual Molecular Characteristics Establishes a New Clade within the Vertebrate Fibrillar Collagen Family

Invertebrate Data Predict an Early Emergence of Vertebrate Fibrillar Collagen Clades and an Anti-incest Model

Collagen fibrillogenesis in tendon development: Current models and regulation of fibril assembly

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